Cross-linking ATP synthase complexes in vivo eliminates mitochondrial cristae

Journal of Cell Science

Volumn 117, Issue 11, 2004, Pages 2333-2343

  Gavin, Paul D ^a   Prescott, Mark ^a   Luff, Susan E ^a   Devenish, Rodney J ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

ATP synthase; Cristae; Cross linking; DsRed; Mitochondria; Yeast

Indexed keywords

HYBRID PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RED FLUORESCENT PROTEIN; TETRAMER;

ARTICLE; CELL GROWTH; CELL LYSATE; CELL ORGANELLE; CELL RESPIRATION; CELL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE ANALYSIS; IN VIVO STUDY; MICROSCOPY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN TARGETING;

CELL DIVISION; CROSS-LINKING REAGENTS; INTRACELLULAR MEMBRANES; LUMINESCENT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTON-TRANSLOCATING ATPASES; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE;

EID: 3042591096     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01074     Document Type: Article

References (46)

1. Allen, R. D. (1995). Membrane tubulation and proton pumps. Protoplasma 189, 1-8.
2. Allen, R. D., Schroeder, C. C. and Fok, A. K. (1989). An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J. Cell Biol. 108, 2233-2240.
3. Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R. A. and Schägger, H. (1998). Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J. 17, 7170-7178.
4. Arselin, G., Giraud, M., Dautant, A., Vaillier, J., Brethes, D., Coulary-Salin, B., Schaeffer, J. and Velours, J. (2003). The GxxxG motif of the transmembrane domain of subunit e is involved in the dimerization/oligomerization of the yeast ATP synthase complex in the mitochondrial membrane. Eur. J. Biochem. 270, 1875-1884.
5. Baird, G. S., Zacharias, D. A. and Tsien, R. Y. (2000). Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc. Natl. Acad. Sci. USA 97, 11984-11989.
6. Bateson, M., Devenish, R. J., Nagley, P. and Prescott, M. (1999). Single Copies of Subunits d, oligomycin-sensitivity conferring protein, and b are present in the Saccharomyces cerevisiae mitochondrial ATP synthase. J. Biol. Chem. 274, 7462-7466.
7. Berger, K. H. and Yaffe, M. P. (2000). Mitochondrial DNA inheritance in Saccharomyces cerevisiae. Trends Microbiol. 8, 508-513.
8. Boyle, G. M., Roucou, X., Nagley, P., Devenish, R. J. and Prescott, M. (1999). Identification of subunit g of yeast mitochondrial F1F0-ATP synthase, a protein required for maximal activity of cyrochrome c oxidase. Eur. J. Biochem. 262, 315-323.
9. Brunner, S., Everard-Gigot, V. and Stuart, R. A. (2002). Su e of the yeast F1F0-ATP synthase forms homo-dimers. J. Biol. Chem. 277, 48484-48489.
10. 1. J. Biol. Chem. 275, 28353-28355.
11. Capaldi, R. A. and Aggeler, R. (2002). Mechanism of the F(1)F(0)-type ATP synthase, a biological rotary motor. Trends Biochem. Sci. 27, 154-160.
12. Cormack, B. P., Bertram, G., Egerton, M., Gow, N. A., Falkow, S. and Brown, A. J. (1997). Yeast-enhanced green fluorescent protein (yEGFP) a reporter of gene expression in Candida albicans. Microbiology 143, 303-311.
13. Dienhart, M., Pfeiffer, K., Schägger, H. and Stuart, R. A. (2002). Formation of the yeast F1F0-ATP symbase dimeric complex does not require the ATPase inhibitor protein, Inh1. J. Biol. Chem. 277, 39289-39295.
14. Egner, A., Jakobs, S. and Hell, S. W. (2002). Fast 100-nm resolution three-dimensional microscope reveals structural plasticity of mitochondria in live yeast. Proc. Natl. Acad. Sci. USA 99, 3370-3375.
15. Frey, T. G. and Mannella, C. A. (2000). The internal structure of mitochondria. Trends Biochem. Sci. 25, 319-324.
16. Gavin, P., Devenish, R.J. and Prescott, M. (2002). An approach for reducing unwanted oligomerisation of DsRed fusion proteins. Biochem. Biophys. Res. Commun. 298, 707-713.
17. Gilkerson, R. W., Selker, J. M. L. and Capaldi, R. A. (2003). The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett. 546, 355-358.
18. Grasso, D. G., Nero, D., Law, R. H., Devenish, R. J. and Nagley, P. (1991). The C-terminal positively charged region of subunit 8 of yeast mitochondrial ATP synthase is required for efficient assembly of this subunit into the membrane F0 sector. Eur. J. Biochem. 199, 203-209.
19. Gumbiowski, K., Cherepanov, D., Muller, M., Panke, O., Promto, P., Winkler, S., Junge, W. and Engelbrecht, S. (2001). F-ATPase: forced full rotation of the rotor despite covalent cross-link with the stator. J. Biol. Chem. 276, 42287-42292.
20. Hanekamp, T., Thorsness, M. K., Rebbapragada, I., Fisher, E. M., Seebart, C., Darland, M. R., Coxbill, J. A., Updike, D. L. and Thorsness, P. E. (2002). Maintenance of mitochondrial morphology is linked to maintenance of the mitochondrial genome in Saccharomyces cerevisiae. Genetics 162, 1147-1156.
21. Hermann, G. J. and Shaw, J. M. (1998). Mitocbondrial dynamics in yeast. Annu. Rev. Cell Dev. Biol. 14, 265-303.
22. Hoffmann, H. P. and Avers, C. J. (1973). Mitochondrion of yeast: ultrastructural evidence for one giant, branched organelle per cell. Science 181, 749-751.
23. Karbowski, M. and Youle, R. J. (2003). Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 10, 870-880.
24. Lauf, U., Lopez, P. and Falk, M. M. (2001). Expression of fluorescently tagged connexins: a novel approach to rescue function of oligomeric DsRed-tagged proteins. FEBS Lett. 498, 11-15.
25. Mannella, C. A., Pfeiffer, D. R., Bradshaw, P. C., Moraru, II, Slepchenko, B., Loew, L. M., Hsieh, C. E., Buttle, K. and Marko, M. (2001). Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications. IUBMB Life 52, 93-100.
26. Mizuno, H., Sawano, A., Eli, P., Hama, H. and Miyawaki, A. (2001). Red fluorescent protein from Discosoma as a fusion tag and a partner for fluorescence resonance energy transfer. Biochemistry 40, 2502-2510.
27. Noji, H., Yasuda, R., Yoshida, M. and Kinosita, K., Jr (1997). Direct observation of the rotation of F1-ATPase. Nature 386, 299-302.
28. Olichon, A., Emorine, L. J., Descoins, E., Pelloquin, L., Brichese, L., Gas, N., Guillou, E., Delettre, C., Valette, A., Hamel, C. P. et al. (2002). The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett. 523, 171-176.
29. O'Malley, C. J., McColl, B. K., Kong, A. M., Ellis, S. L., Wijayaratnam, A. P., Sambrook, J. and Mitchell, C. A. (2001). Mammalian inositol polyphosphate 5-phosphatase II can compensate for the absence of all three yeast Sac1-like-domain-containing 5-phosphatases. Biochem. J. 355, 805-817.
30. Paumard, P., Arselin, G., Vaillier, J., Chaignepain, S., Bathany, K., Schmitter, J. M., Brethes, D. and Velours, J. (2002a). Two ATP synthases can be linked through subunits i in the inner mitochondrial membrane of Saccharomyces cerevisiae. Biochemistry 41, 10390-10396.
31. Paumard, P., Vaillier, J., Coulary, B., Schaeffer, J., Soubannier, V., Mueller, D. M., Brethes, D., di Rago, J. P. and Velours, J. (2002b). The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21, 221-230.
32. Prescott, M., Nowakowski, S., Gavin, P., Nagley, P., Whisstock, J. C. and Devenish, R. J. (2003). Subunit gamma-green fluorescent protein fusions are functionally incorporated into mitochondrial F1F0-ATP synthase, arguing against a rigid cap structure at the top of F1. J. Biol. Chem. 278, 251-256.
33. Roeder, A. D., Hermann, G. J., Keegan, B. R., Thatcher, S. A. and Shaw, J. M. (1998). Mitochondrial inheritance is delayed in Saccharomyces cerevisiae cells lacking the serine/threonine phosphatase PTC1. Mol. Biol. Cell 9, 917-930.
34. Sacchetti, A., Subramaniam, V., Jovin, T. M. and Alberti, S. (2002). Oligomerization of DsRed is required for the generation of a functional red fluorescent chromophore. FEBS Lett. 525, 13-19.
35. Schägger, H. (2001). Respiratory chain supercomplexes. IUBMB Life 52, 119-128.
36. Schägger, H. (2002). Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 1555, 154-159.
37. Schägger, H., Cramer, W. A. and von Jagow, G. (1994). Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217, 220-230.
38. Schägger, H. and Pfeiffer, K. (2000). Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19, 1777-1783.
39. Scorrano, L., Ashiya, M., Buttle, K., Weiler, S., Oakes, S. A., Mannella, C. A. and Korsmeyer, S. J. (2002). A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2, 55-67.
40. Shaw, J. M. and Nunnari, J. (2002). Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12, 178-184.
41. Shepard, K. A. and Yaffe, M. P. (1999). The yeast dynamin-like protein, Mgm1p, functions on the mitochondrial outer membrane to mediate mitochondrial inheritance. J. Cell Biol. 144, 711-720.
42. Soubannier, V., Rusconi, F., Vaillier, J., Arselin, G., Chaignepain, S., Graves, P. V., Schmitter, J. M., Zhang, J. L., Mueller, D. and Velours, J. (1999). The second stalk of the yeast ATP synthase complex: identification of subunits showing cross-links with known positions of subunit 4 (subunit b). Biochemistry 38, 15017-15024.
43. Soubannier, V., Vaillier, J., Paumard, P., Coulary, B., Schaeffer, J. and Velours, J. (2002). In the absence of the first membrane-spanning segment of subunit 4(b), the yeast ATP synthase is functional but does not dimerize or oligomerize. J. Biol. Chem. 277, 10739-10745.
44. Spannagel, C., Vaillier, J., Arselin, G., Graves, P. V., Grandier-Vazeille, X. and Velours, J. (1998). Evidence of a subunit 4 (subunit b) dimer in favor of the proximity of ATP synthase complexes in yeast inner mitochondrial membrane. Biochim. Biophys. Acta 1414, 260-264.
45. Straffon, A. F., Prescott, M., Nagley, P. and Devenish, R. J. (1998). The assembly of yeast mitochondrial ATP synthase: subunit depletion in vivo suggests ordered assembly of the stalk subunits b, OSCP and d. Biochim. Biophys. Acta 1371, 157-162.
46. Wong, E. D., Wagner, J. A., Scott, S. V., Okreglak, V., Holewinske, T. J., Cassidy-Stone, A. and Nunnari, J. (2003). The intramitochondrial dynamin-related GTPase, Mgm1p, is a component of a protein complex that mediates mitochondrial fusion. J. Cell Biol. 160, 303-311.